The genetic basis of rapidly evolving male genital morphology in Drosophila

Genetics

Volumn 189, Issue 1, 2011, Pages 357-374

  Masly, John P ^a,b   Dalton, Justin E ^a   Srivastava, Sudeep ^a   Chen, Liang ^a   Arbeitman, Michelle N ^a,c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MAURITIANA; DROSOPHILA MELANOGASTER; DROSOPHILA SECHELLIA; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENOTYPE; INSECT DEVELOPMENT; INSECT GENETICS; INTERSPECIFIC HYBRIDIZATION; INTROGRESSION; LARVA; MALE; MALE GENITAL SYSTEM; NEUROHYPOPHYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ALTERNATIVE SPLICING; ANIMALS; BIOLOGICAL EVOLUTION; CHIMERA; CROSSES, GENETIC; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENITALIA, MALE; IMAGINAL DISCS; INSULIN; MALE; MORPHOGENESIS; PHENOTYPE; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

DROSOPHILA MAURITIANA; DROSOPHILA MELANOGASTER; DROSOPHILA SECHELLIA; HEXAPODA;

EID: 80052666671     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.130815     Document Type: Article

References (123)

1. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram, 2004 Image Processing with Image J. Biophotonics International 11: 36-42.
2. Abzhanov, A., M. Protas, B. R. Grant, P. R. Grant, and C. J. Tabin, 2004 Bmp4 and morphological variation of beaks in Darwin's finches. Science 305: 1462-1465.
3. Abzhanov, A., W. P. Kuo, C. Hartmann, B. R. Grant, P. R. Grant et al., 2006 The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 442: 563-567.
4. Andres, A. J., and C. S. Thummel, 1994 Methods for quantitative analysis of transcription in larvae and prepupae. Methods Cell Biol. 44: 565-573.
5. Anjum, R., and J. Blenis, 2008 The RSK family of kinases: emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol. 9: 747-758.
6. Ashburner, M., K. G. Golic, and R. S. Hawley, 2005 Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
7. Barmina, O., and A. Kopp, 2007 Sex-specific expression of a HOX gene associated with rapid morphological evolution. Dev. Biol. 311: 277-286.
8. Bathke, A. C., S. W. Harrar, and L. V. Madden, 2008 How to compare small multivariate samples using nonparametric tests. Comput. Stat. Data Anal. 52: 4951-4965.
9. Baxter, C. E., M. M. Costa, and E. S. Coen, 2007 Diversification and co-option of RAD-like genes in the evolution of floral asymmetry. Plant J. 52: 105-113.
10. Beldade, P., P. M. Brakefield, and A. D. Long, 2002 Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415: 315-318.
11. Boll, W., and M. Noll, 2002 The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129: 5667-5681.
12. Burtis, K. C., and B. S. Baker, 1989 Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56: 997-1010.
13. Catchpole, R. D. J., 1994 Wing length is not the best predictor of body size. Drosoph. Inf. Serv. 75: 84-86.
14. Catron, D. J., and M. A. F. Noor, 2008 Gene expression disruptions of organism vs. organ in Drosophila species hybrids. PLoS ONE 3: e3009.
15. Chatterjee, S. S., L. D. Uppendahl, M. A. Chowdhury, P.-L. Ip, and M. L. Siegal, 2011 The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development in Drosophila. Development 138: 1099-1109.
16. Chen, P., A. Rodriguez, R. Erskine, T. Thach, and J. M. Abrams, 1998 Dredd, a novel effector of the apoptosis activators Reaper, Grim, and Hid in Drosophila. Dev. Biol. 201: 202-216.
17. Chen, Y., T. Souaiaia, and T. Chen, 2009 PerM: efficient mapping of short sequencing reads with periodic full sensitive spaced seeds. Bioinformatics 25: 2514-2521.
18. Christiansen, A. E., E. L. Keisman, S. M. Ahmad, and B. S. Baker, 2002 Sex comes in from the cold: the integration of sex and pattern. Trends Genet. 18: 510-516.
19. Clark, R. M., T. N. Wagler, P. Quijada, and J. Doebley, 2006 A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat. Genet. 38: 594-597.
20. Corley, S. B., R. Carpenter, L. Copsey, and E. Coen, 2005 Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc. Natl. Acad. Sci. USA 102: 5068-5073.
21. Costa, M., S. Fox, A. I. Hanna, C. Baxter, and E. Coen, 2005 Evolution of regulatory interactions controlling floral asymmetry. Development 132: 5093-5101.
22. Coyne, J. A., 1983 Genetic basis of differences in genital morphology among three sibling species of Drosophila. Evolution 37: 1101-1118.
23. Coyne, J. A., 1993 The genetics of an isolating mechanism between two sibling species of Drosophila. Evolution 47: 778-788.
24. Coyne, J. A., and M. Kreitman, 1986 Evolutionary genetics of two sibling species, Drosophila simulans and D. sechellia. Evolution 40: 673-691.
25. Coyne, J. A., and H. A. Orr, 2004 Speciation. Sinauer Associates, Sunderland, MA.
26. Coyne, J. A., J. Rux, and J. R. David, 1991 Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives. Genet. Res. 57: 113-122.
27. Cretekos, C. J., Y. Wang, E. D. Green, J. F. Martin, J. J. T. Rasweiler et al., 2008 Regulatory divergence modifies limb length between mammals. Genes Dev. 22: 141-151.
28. Da, L., R. Carpenter, L. Copsey, C. Vincent, J. Clark et al., 1999 Control of organ asymmetry in flowers of Antirrhinum. Cell 99: 367-376.
29. Doebley, J., A. Stec, and L. Hubbard, 1997 The evolution of apical dominance in maize. Nature 386: 485-488.
30. Eberhard, W. G., 1985 Sexual Selection and Animal Genitalia. Harvard University Press, Cambridge, MA.
31. Eberhard, W. G., 2008 Static allometry and animal genitalia. Evolution 63: 48-66.
32. Eberhard, W. G., and N. Ramirez, 2004 Functional morphology of the male genitalia of four species of Drosophila: failure to confirm both the lock and key and male-female conflict predictions. Ann. Entomol. Soc. Am. 97: 1007-1017.
33. Ehrensperger, P., 1983 Die Entwicklung der bisexuellen Anlage der Genitalien und Analien, untersucht an verschiedenen Geschelchtsmutanten der Taufliege Drosophila melanogaster. Inaugural Dissertation, University of Zurich, Zurich.
34. Epper, F., 1983a The evagination of the genital imaginal discs of Drosophila melanogaster 1. Morphogenesis of the female genital disc. Rouxs Arch. Dev. Biol. 192: 275-279.
35. Epper, F., 1983b The evagination of the genital imaginal discs of Drosophila melanogaster 2. Morphogenesis of the inter sexual genital disc of the mutant doublesex dominant DSX-D. Rouxs Arch. Dev. Biol. 192: 280-284.
36. Erwin, D. H., and E. H. Davidson, 2009 The evolution of hierarchical gene regulatory networks. Nat. Rev. Genet. 10: 141-148.
37. Estrada, B., F. Casares, and E. Sanchez-Herrero, 2003 Development of the genitalia in Drosophila melanogaster. Differentiation 71: 299-310.
38. Franke, A., and B. S. Baker, 1999 The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. Mol. Cell 4: 117-122.
39. Fraser, G. J., C. D. Hulsey, R. F. Bloomquist, K. Uyesugi, N. R. Manley et al., 2009 An ancient gene network is co-opted for teeth on old and new jaws. PLoS Biol. 7: e31.
40. Galego, L., and J. Almeida, 2002 Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev. 16: 880-891.
41. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling et al., 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
42. Goldman, T. D., and M. N. Arbeitman, 2007 Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet. 3: e216.
43. Gompel, N., B. Prud'homme, P. J. Wittkopp, V. A. Kassner, and S. B. Carroll, 2005 Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481-487.
44. Graze, R. M., L. M. McIntyre, B. J. Main, M. L. Wayne, and S. V. Nuzhdin, 2009 Regulatory divergence in Drosophila melanogaster and D. simulans, a genome-wide analysis of allele-specific expression. Genetics 183: 547-561.
45. Grewal, S. S., 2009 Insulin/TOR signaling in growth and homeostasis: a view from the fly world. Int. J. Biochem. Cell Biol. 41: 1006-1010.
46. Hannus, M., F. Feiguin, C.-P. Heisenberg, and S. Eaton, 2002 Planar cell polarization requires Widerborst, a B' regulatory subunit of protein phosphatase 2A. Development 129: 3493-3503.
47. Hay, A., and M. Tsiantis, 2006 The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 38: 942-947.
48. Hietakangas, V., and S. M. Cohen, 2009 Regulation of tissue growth through nutrient sensing. Annu. Rev. Genet. 43: 389-410.
49. Hill-Burns, E. M., and A. G. Clark, 2010 Functional regulatory divergence of the innate immune system in interspecific Drosophila hybrids. Mol. Biol. Evol. 27: 2596-2605.
50. Hinman, V. F., and E. H. Davidson, 2007 Evolutionary plasticity of developmental gene regulatory network architecture. Proc. Natl. Acad. Sci. USA 104: 19404-19409.
51. Hrycaj, S., J. Chesebro, and A. Popadic, 2010 Functional analysis of Scr during embryonic and post-embryonic development in the cockroach, Periplaneta americana. Dev. Biol. 341: 324-334.
52. Hsu, T. C., 1949 The external genital apparatus of male Drosophilae in relation to systematics. Univ Texas Pub 4920: 80-142.
53. Hubbard, L., P. McSteen, J. Doebley, and S. Hake, 2002 Expression patterns and mutant phenotype of teosinte branched 1 correlate with growth suppression in maize and teosinte. Genetics 162: 1927-1935.
54. Jacinto, A., W. Wood, S. Woolner, C. Hiley, L. Turner et al., 2002 Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12: 1245-1250.
55. Jagadeeshan, S., and R. S. Singh, 2006 A time-sequence functional analysis of mating behaviour and genital coupling in Drosophila: role of cryptic female choice and male sex-drive in the evolution of genitalia. J. Evol. Biol. 19: 1058-1070.
56. Khalturin, K., F. Anton-Erxleben, S. Sassmann, J. Wittlieb, G. Hemmrich et al., 2008 A novel gene family controls speciesspecific morphological traits in Hydra. PLoS Biol. 6: e278.
57. Kijimoto, T., J. Andrews, and A. P. Moczek, 2010 Programed cell death shapes the expression of horns within and between species of horned beetles. Evol. Dev. 12: 449-458.
58. Kim, M., J. H. Lee, H. Koh, S. Y. Lee, C. Jang et al., 2006 Inhibition of ERK-MAP kinase signaling by RSK during Drosophila development. EMBO J. 25: 3056-3067.
59. Klebes, A., B. Biehs, F. Cifuentes, and T. B. Kornberg, 2002 Expression profiling of Drosophila imaginal discs. Genome Biol 3: RESEARCH0038.
60. Kliman, R. M., P. Andolfatto, J. A. Coyne, F. Depaulis, M. Kreitman et al., 2000 The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156: 1913-1931.
61. Kopp, A., I. Duncan, D. Godt, and S. B. Carroll, 2000 Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408: 553-559.
62. Kuhl, F. P., and C. R. Giardina, 1982 Elliptical Fourier features of a closed contour. Comp. Graph Image Process 18: 236-258.
63. Landry, C. R., P. J. Wittkopp, C. H. Taubes, J. M. Ranz, A. G. Clark et al., 2005 Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171: 1813-1822.
64. Laurie, C. C., J. R. True, J. Liu, and J. M. Mercer, 1997 An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana. Genetics 145: 339-348.
65. Lebo, M. S., L. E. Sanders, F. Sun, and M. N. Arbeitman, 2009 Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis. BMC Genomics 10: 80.
66. Li, X., A. Scuderi, A. Letsou, and D. M. Virshup, 2002 B56-associated protein phosphatase 2A is required for survival and protects from apoptosis in Drosophila melanogaster. Mol. Cell. Biol. 22: 3674-3684.
67. Liu, J., J. M. Mercer, L. F. Stam, G. C. Gibson, Z.-B. Zeng et al., 1996 Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics 142: 1129-1145.
68. Loehlin, D. W., D. C. S. G. Oliveira, R. Edwards, J. D. Giebel, M. E. Clark et al., 2010 Non-coding changes cause sex-specific wing size differences between closely related species of Nasonia. PLoS Genet. 6: e1000821.
69. Lu, X., J. A. Shapiro, C.-T. Ting, Y. Li, C. Li et al., 2010 Genomewide mis-expression of X-linked vs. autosomal genes associated with hybrid male sterility. Genome Res. 20: 1097-1102.
70. Luo, D., R. Carpenter, C. Vincent, L. Copsey, and E. Coen, 1996 Origin of floral asymmetry in Antirrhinum. Nature 383: 794-799.
71. MacDonald, S. J., and D. B. Goldstein, 1999 A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153: 1683-1699.
72. Magie, C. R., M. R. Meyer, M. S. Gorsuch, and S. M. Parkhurst, 1999 Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126: 5353-5364.
73. Mallarino, R., P. R. Grant, B. R. Grant, A. Herrel, W. P. Kuo et al., 2011 Two developmental modules establish 3D beak-shape variation in Darwin's finches. Proc. Natl. Acad. Sci. USA 108: 4057-4062.
74. Malone, J., and P. Michalak, 2008 Gene expression analysis of the ovary of hybrid females of Xenopus laevis and X. muelleri. BMC Evol. Biol. 8: 82.
75. Malone, J. H., T. H. Chrzanowski, and P. Michalak, 2007 Sterility and gene expression in hybrid males of Xenopus laevis and X. muelleri. PLoS ONE 2: e781.
76. Martin-Belmonte, F., A. Gassama, A. Datta, W. Yu, U. Rescher et al., 2007 PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128: 383-397.
77. Masly, J. P., and D. C. Presgraves, 2007 High-resolution genomewide dissection of the two rules of speciation in Drosophila. PLoS Biol. 5: 1890-1898.
78. Mayer-Jaekel, R. E., S. Baumgartner, G. Bilbe, H. Ohkura, D. M. Glover et al., 1992 Molecular cloning and developmental expression of the catalytic and 65- kDa regulatory subunits of protein phosphatase 2A in Drosophila. Mol. Biol. Cell 3: 287-298.
79. McCauley, D. W., and M. Bronner-Fraser, 2006 Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441: 750-752.
80. McGregor, A. P., V. Orgogozo, I. Delon, J. Zanet, D. G. Srinivasan et al., 2007 Morphological evolution through multiple cisregulatory mutations at a single gene. Nature 448: 587-590.
81. McManus, C. J., J. D. Coolon, M. O'Duff, J. Eipper-Mains, B. R. Graveley et al., 2010 Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 20: 816-825.
82. Meulemans, D., and M. Bronner-Fraser, 2002 Amphioxus and lamprey AP-2 genes: implications for neural crest evolution and migration patterns. Development 129: 4953-4962.
83. Michalak, P., and M. A. Noor, 2004 Association of misexpression with sterility in hybrids of Drosophila simulans and D. mauritiana. J. Mol. Evol. 59: 277-282.
84. Moczek, A. P., and D. J. Rose, 2009 Differential recruitment of limb patterning genes during development and diversification of beetle horns. Proc. Natl. Acad. Sci. USA 106: 8992-8997.
85. Moehring, A. J., K. C. Teeter, and M. A. Noor, 2007 Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. Mol. Biol. Evol. 24: 137-145.
86. Pinal, N., D. C. I. Goberdhan, L. Collinson, Y. Fujita, I. M. Cox et al., 2006 Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr. Biol. 16: 140-149.
87. Price, C. S., C. H. Kim, C. J. Gronlund, and J. A. Coyne, 2001 Cryptic reproductive isolation in the Drosophila simulans species complex. Evolution 55: 81-92.
88. Prud'homme, B., N. Gompel, A. Rokas, V. A. Kassner, T. M. Williams et al., 2006 Repeated morphological evolution through cisregulatory changes in a pleiotropic gene. Nature 440: 1050-1053.
89. Rasband, W. S., 1997-2010 ImageJ. National Institutes of Health, Bethesda, MD.
90. Reed, R. D., and M. S. Serfas, 2004 Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Curr. Biol. 14: 1159-1166.
91. Renaut, S., A. W. Nolte, and L. Bernatchez, 2009 Gene expression divergence and hybrid misexpression between lake whitefish species pairs (Coregonus spp. Salmonidae). Mol. Biol. Evol. 26: 925-936.
92. Rieseberg, L. H., M. A. Archer, and R. K. Wayne, 1999 Transgressive segregation, adaptation and speciation. Heredity 83 (4): 363-372.
93. Robertson, H. M., 1988 Mating assymettries and phylogeny in the Drosophila melanogaster species complex. Pac. Sci. 42: 72-80.
94. Ronshaugen, M., N. McGinnis, and W. McGinnis, 2002 Hox protein mutation and macroevolution of the insect body plan. Nature 415: 914-917.
95. Rosas, U., N. H. Barton, L. Copsey, P. Barbier de Reuille, and E. Coen, 2010 Cryptic variation between species and the basis of hybrid performance. PLoS Biol. 8: e1000429.
96. Roux, P. P., and J. Blenis, 2004 ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68: 320-344.
97. Sánchez, L., and I. Guerrero, 2001 The development of the Drosophila genital disc. Bioessays 23: 698-707.
98. Shingleton, A. W., J. Das, L. Vinicius, and D. L. Stern, 2005 The temporal requirements for insulin signaling during development in Drosophila. PLoS Biol. 3: e289.
99. Shingleton, A. W., C. M. Estep, M. V. Driscoll, and I. Dworkin, 2009 Many ways to be small: different environmental regulators of size generate distinct scaling relationships in Drosophila melanogaster. Proc. Biol. Sci. B 276: 2625-2633.
100. Shirataki, H., R. Futahashi, and H. Fujiwara, 2010 Speciesspecific coordinated gene expression and trans-regulation of larval color pattern in three swallowtail butterflies. Evol. Dev. 12: 305-314.
101. Smyth, G. K., 2005 Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor, edited by Gentleman V. C. R., S. Dudoit, R. Irizarry, and W. Huber, pp. 397-420. Springer, New York.
102. Smyth, G. K., and T. Speed, 2003 Normalization of cDNA microarray data. Methods 31: 265-273.
103. Srivastava, S., and L. Chen, 2010 A two-parameter generalized Poisson model to improve the analysis of RNA-seq data. Nucleic Acids Res. 38: e170.
104. Stern, D. L., 1998 A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396: 463-466.
105. Storey, J. D., 2003 The positive flase discovery rate: A Bayesian interpretation and the q-value. Ann. Stat. 31: 2013-2035.
106. Strutt, D. I., U. Weber, and M. Mlodzik, 1997 The role of RhoA in tissue polarity and Frizzled signalling. Nature 387: 292-295.
107. Sucena, E., and D. L. Stern, 2000 Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc. Natl. Acad. Sci. USA 97: 4530-4534.
108. Tamura, K., S. Subramanian, and S. Kumar, 2004 Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21: 36-44.
109. R Development Core Team, 2010 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
110. Tirosh, I., S. Reikhav, A. A. Levy, and N. Barkai, 2009 A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659-662.
111. True, J. R., J. M. Mercer, and C. C. Laurie, 1996 Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142: 507-523.
112. Vereshchagina, N., and C. Wilson, 2006 Cytoplasmic activated protein kinase Akt regulates lipid-droplet accumulation in Drosophila nurse cells. Development 133: 4731-4735.
113. Wang, K., D. Singh, Z. Zeng, S. J. Coleman, Y. Huang et al., 2010 MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res. 38: e178.
114. Wasik, B. R., D. J. Rose, and A. P. Moczek, 2010 Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner. Evol. Dev. 12: 353-362.
115. Wasik, B. R., and A. P. Moczek, 2011 Decapentaplegic (dpp) regulates the growth of a morphological novelty, beetle horns. Dev. Genes Evol. 221: 17-27.
116. Welch, B. L., 1947 The generalization of "Student's" problem when several different population variances are involved. Biometrika 34: 25-38.
117. Werner, T., S. Koshikawa, T. M. Williams, and S. B. Carroll, 2010 Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464: 1143-1148.
118. Wittkopp, P. J., B. L. Williams, J. E. Selegue, and S. B. Carroll, 2003 Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc. Natl. Acad. Sci. USA 100: 1808-1813.
119. Wittkopp, P. J., B. K. Haerum, and A. G. Clark, 2004 Evolutionary changes in cis and trans gene regulation. Nature 430: 85-88.
120. Wittkopp, P. J., B. K. Haerum, and A. G. Clark, 2008 Regulatory changes underlying expression differences within and between Drosophila species. Nat. Genet. 40: 346-350.
121. Wittkopp, P. J., E. E. Stewart, L. L. Arnold, A. H. Neidert, B. K. Haerum et al., 2009 Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326: 540-544.
122. Yan, J., Q. Lu, X. Fang, and P. N. Adler, 2009 Rho1 has multiple functions in Drosophila wing planar polarity. Dev. Biol. 333: 186-199.
123. Zeng, Z.-B., J. Liu, L. F. Stam, C.-H. Kao, J. M. Mercer et al., 2000 Genetic architecture of a morphological shape difference between two Drosophila species. Genetics 154: 299-310.